A resident of the Apache Reservation in Terra Mesa, New Mexico, John's father, Benjamin Blackwolf, was killed by federal agents at Wounded Knee when violence broke out. Becoming a police officer, John also taught at the reservation's school, and was a regular guest speaker at seminars on Native American culture. An expert tracker, John was, on occasion, called upon by Sheriff Jim Rhodes to help in the search for lost hikers and campers. John also had a criminal record, though mostly for charges related to his activism, such as heading illegal demonstrations.

In 2006, when five college students are killed in an empty house, the murderers having utilized old Native war rituals to torture them beforehand, John is approached by the Sheriff Rhodes and the BAU for aid. Brought to the house, John discerns there was a sixth victim, who was taken by two attackers, while at least another six murdered the remaining students. John also realizes that it was not Native Americans who committed the murders, but copycats, as the war rituals they used to mutilate the students were a random mixture of ones performed by different tribes. The killers had knowledge of Native American traditions, but it was mixed and basic. From the start, there is some friction between John and Hotch.

John is later present when the BAU gives its profile to the police, repeating his belief that the killers are not actual Native Americans, but confused imitators. When the abducted victim, Ingrid Griesen, a member of the cult responsible for the massacres, is found (having been abducted by men hired by her father, who had intended to reverse the cult's brainwashing by bringing her to a deprogrammer) John is brought in to talk her at the Minton house, the scene of the cult's latest slaughter. As Ingrid begins rambling about how "Grandfather" had showed her the way, she calls Hotch and all other Caucasians trespassers, and refers to John as a traitor, and not a true Apache. John grows angered by Ingrid's words, especially after she refers to Grandfather as the Native American messiah, and, shoving the blood-caked stuffed animal of a young victim into her face, yells that she has been lied to and knows nothing of his people, causing Ingrid to blurt out Grandfather's whereabouts, the Deadlands.

John and the BAU track down Grandfather, revealed to be a man named Jackson Cally, to an abandoned hotel. During questioning, Jackson claims his followers are out hunting, and reveals his racism-fueled intent to spark a war between Caucasians and Native Americans. When Jackson refers to him and his father as nothing but savage animals, John has to be restrained from attacking him by Morgan. The team are soon able to discern what the cult's next target is, the reservation's school, which they intend to massacre. The cult would make the attack look like the work of a local group known as the American Defense League, by using firearms stolen from the home of the murdered Roy Minton, who was the leader of the organization. John and Hotch reach the school first, and have the children and teacher, Jane Bear, hide in the basement, while they take care of the cult, John convincing Hotch not to use his guns. After knocking out one assailant, John fatally wounds another in a knife fight, and is saved from two others by Hotch, who is forced to use his sidearm. Rounding up the surviving cultists, John and Hotch tie them up and await the arrival of the police and the rest of the BAU. Despite John disapproving of Hotch using his gun, he and Hotch bid farewell on amiable terms.